Skip to main content
Top
Published in: BMC Infectious Diseases 1/2014

Open Access 01-12-2014 | Research article

Leishmania amazonensis infection impairs dendritic cell migration from the inflammatory site to the draining lymph node

Authors: Micely DR Hermida, Priscila G Doria, Angela MP Taguchi, José O Mengel, Washington LC dos-Santos

Published in: BMC Infectious Diseases | Issue 1/2014

Login to get access

Abstract

Background

In vitro studies show that Leishmania infection decreases the adhesion of inflammatory phagocytes to connective tissue by a mechanism dependent on the modulation of integrin function. However, we know little about the influence of this reduction in leukocyte adhesion on parasite dissemination from the infection site.

Methods

In this work, we used a model of chronic peritonitis induced by thioglycollate to study the effect of L. amazonensis infection on the ability of inflammatory phagocyte populations to migrate from an inflammatory site to the draining lymph node. Uninfected or Leishmania-infected thioglycollate-elicited peritoneal exudate cells were transferred from C57BL/6 to BALB/c mice or from Ly5.1+ to Ly5.1- mice. The transferred cells were injected into the peritoneal cavity and tracked to the draining lymph node.

Results

Migrating cells corresponded to approximately 1% of the injected leukocytes. The proportion of migrating CD11b+CD11c+ (myeloid dendritic cell) was lower after incubation with Leishmania (1.3 to 2.6 times lower in the experiments using C57BL/6 to BALB/c animals and 2.7 to 3.4 times lower in the experiments using Ly5.1+ to Ly5.1- animals) than after leukocyte incubation with medium alone (P < 0.01). There was no consistent decrease in the migration of CD11b+F4/80+ (macrophage) or SSChi GR-1+ (neutrophil) populations.

Conclusions

Coincubation with Leishmania changes the migratory pattern of dendritic cells in vivo. Such changes in dendritic cell migration may be associated with immunological events that maintain inflammation at the sites of infection.
Appendix
Available only for authorised users
Literature
1.
go back to reference Guarga JL, Lucientes J, Peribáñez MA, Molina R, Gracia MJ, Castillo JA: Experimental infection of Phlebotomus perniciosus and determination of the natural infection rates of Leishmania infantum in dogs. Acta Trop. 2000, 77: 203-207.CrossRefPubMed Guarga JL, Lucientes J, Peribáñez MA, Molina R, Gracia MJ, Castillo JA: Experimental infection of Phlebotomus perniciosus and determination of the natural infection rates of Leishmania infantum in dogs. Acta Trop. 2000, 77: 203-207.CrossRefPubMed
3.
go back to reference Moll H, Fuchs H, Blank C, Röllinghoff M: Langerhans cells transport Leishmania major from the infected skin to the draining lymph node for presentation to antigen-specific T cells. Eur J Immunol. 1993, 23: 1595-1601.CrossRefPubMed Moll H, Fuchs H, Blank C, Röllinghoff M: Langerhans cells transport Leishmania major from the infected skin to the draining lymph node for presentation to antigen-specific T cells. Eur J Immunol. 1993, 23: 1595-1601.CrossRefPubMed
4.
go back to reference Muraille E, De Trez C, Pajak B, Torrentera FA, De Baetselier P, Leo O, Carlier Y: Amastigote load and cell surface phenotype of infected cells from lesions and lymph nodes of susceptible and resistant mice infected with leishmania major. Infect Immun. 2003, 71: 2704-2715.CrossRefPubMedPubMedCentral Muraille E, De Trez C, Pajak B, Torrentera FA, De Baetselier P, Leo O, Carlier Y: Amastigote load and cell surface phenotype of infected cells from lesions and lymph nodes of susceptible and resistant mice infected with leishmania major. Infect Immun. 2003, 71: 2704-2715.CrossRefPubMedPubMedCentral
5.
go back to reference Peters NC, Kimblin N, Secundino N, Kamhawi S, Lawyer P, Sacks DL: Vector transmission of leishmania abrogates vaccine-induced protective immunity. PLoS Pathog. 2009, 5: e1000484-CrossRefPubMedPubMedCentral Peters NC, Kimblin N, Secundino N, Kamhawi S, Lawyer P, Sacks DL: Vector transmission of leishmania abrogates vaccine-induced protective immunity. PLoS Pathog. 2009, 5: e1000484-CrossRefPubMedPubMedCentral
6.
7.
go back to reference León B, López-Bravo M, Ardavín C: Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity. 2007, 26: 519-531.CrossRefPubMed León B, López-Bravo M, Ardavín C: Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity. 2007, 26: 519-531.CrossRefPubMed
8.
go back to reference Lemos de Souza V, Ascenção Souza J, Correia Silva TM, Sampaio Tavares Veras P, Rodrigues de-Freitas LA: Different Leishmania species determine distinct profiles of immune and histopathological responses in CBA mice. Microbes Infect. 2000, 2: 1807-1815.CrossRefPubMed Lemos de Souza V, Ascenção Souza J, Correia Silva TM, Sampaio Tavares Veras P, Rodrigues de-Freitas LA: Different Leishmania species determine distinct profiles of immune and histopathological responses in CBA mice. Microbes Infect. 2000, 2: 1807-1815.CrossRefPubMed
9.
go back to reference Veress B, Omer A, Satir AA, Hassan El AM: Morphology of the spleen and lymph nodes in fatal visceral leishmaniasis. Immunology. 1977, 33: 605-610.PubMed Veress B, Omer A, Satir AA, Hassan El AM: Morphology of the spleen and lymph nodes in fatal visceral leishmaniasis. Immunology. 1977, 33: 605-610.PubMed
11.
go back to reference Carvalhal DGF, Barbosa A, D'El-Rei Hermida M, Clarencio J, Pinheiro NF, Veras PST, Dos-Santos WLC: The modelling of mononuclear phagocyte—connective tissue adhesion in vitro: application to disclose a specific inhibitory effect of Leishmania infection. Exp Parasitol. 2004, 107: 189-199.CrossRefPubMed Carvalhal DGF, Barbosa A, D'El-Rei Hermida M, Clarencio J, Pinheiro NF, Veras PST, Dos-Santos WLC: The modelling of mononuclear phagocyte—connective tissue adhesion in vitro: application to disclose a specific inhibitory effect of Leishmania infection. Exp Parasitol. 2004, 107: 189-199.CrossRefPubMed
12.
go back to reference Pinheiro NF, Hermida MDR, Macedo MP, Mengel J, Bafica A, dos-Santos WLC: Leishmania Infection Impairs 1-Integrin Function and Chemokine Receptor Expression in Mononuclear Phagocytes. Infect Immun. 2006, 74: 3912-3921.CrossRefPubMedPubMedCentral Pinheiro NF, Hermida MDR, Macedo MP, Mengel J, Bafica A, dos-Santos WLC: Leishmania Infection Impairs 1-Integrin Function and Chemokine Receptor Expression in Mononuclear Phagocytes. Infect Immun. 2006, 74: 3912-3921.CrossRefPubMedPubMedCentral
13.
go back to reference Sozzani S, Sallusto F, Luini W, Zhou D, Piemonti L, Allavena P, Van Damme J, Valitutti S, Lanzavecchia A, Mantovani A: Migration of dendritic cells in response to formyl peptides, C5a, and a distinct set of chemokines. J Immunol. 1995, 155: 3292-3295.PubMed Sozzani S, Sallusto F, Luini W, Zhou D, Piemonti L, Allavena P, Van Damme J, Valitutti S, Lanzavecchia A, Mantovani A: Migration of dendritic cells in response to formyl peptides, C5a, and a distinct set of chemokines. J Immunol. 1995, 155: 3292-3295.PubMed
14.
go back to reference Randolph GJ, Angeli V, Swartz MA: Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat Rev Immunol. 2005, 5: 617-628.CrossRefPubMed Randolph GJ, Angeli V, Swartz MA: Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat Rev Immunol. 2005, 5: 617-628.CrossRefPubMed
15.
go back to reference Palframan RT, Jung S, Cheng G, Weninger W, Luo Y, Dorf M, Littman DR, Rollins BJ, Zweerink H, Rot A, Andrian von UH: Inflammatory chemokine transport and presentation in HEV: a remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues. J Exp Med. 2001, 194: 1361-1373.CrossRefPubMedPubMedCentral Palframan RT, Jung S, Cheng G, Weninger W, Luo Y, Dorf M, Littman DR, Rollins BJ, Zweerink H, Rot A, Andrian von UH: Inflammatory chemokine transport and presentation in HEV: a remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues. J Exp Med. 2001, 194: 1361-1373.CrossRefPubMedPubMedCentral
16.
go back to reference Janatpour MJ, Hudak S, Sathe M, Sedgwick JD, McEvoy LM: Tumor necrosis factor-dependent segmental control of MIG expression by high endothelial venules in inflamed lymph nodes regulates monocyte recruitment. J Exp Med. 2001, 194: 1375-1384.CrossRefPubMedPubMedCentral Janatpour MJ, Hudak S, Sathe M, Sedgwick JD, McEvoy LM: Tumor necrosis factor-dependent segmental control of MIG expression by high endothelial venules in inflamed lymph nodes regulates monocyte recruitment. J Exp Med. 2001, 194: 1375-1384.CrossRefPubMedPubMedCentral
17.
go back to reference Leon B, Ardavin C: Monocyte migration to inflamed skin and lymph nodes is differentially controlled by L-selectin and PSGL-1. Blood. 2008, 111: 3126-3130.CrossRefPubMed Leon B, Ardavin C: Monocyte migration to inflamed skin and lymph nodes is differentially controlled by L-selectin and PSGL-1. Blood. 2008, 111: 3126-3130.CrossRefPubMed
18.
19.
go back to reference Bellingan GJ, Caldwell H, Howie SE, Dransfield I, Haslett C: In vivo fate of the inflammatory macrophage during the resolution of inflammation: inflammatory macrophages do not die locally, but emigrate to the draining lymph nodes. J Immunol. 1996, 157: 2577-2585.PubMed Bellingan GJ, Caldwell H, Howie SE, Dransfield I, Haslett C: In vivo fate of the inflammatory macrophage during the resolution of inflammation: inflammatory macrophages do not die locally, but emigrate to the draining lymph nodes. J Immunol. 1996, 157: 2577-2585.PubMed
20.
go back to reference Steigerwald M, Moll H: Leishmania major modulates chemokine and chemokine receptor expression by dendritic cells and affects their migratory capacity. Infect Immun. 2005, 73: 2564-2567.CrossRefPubMedPubMedCentral Steigerwald M, Moll H: Leishmania major modulates chemokine and chemokine receptor expression by dendritic cells and affects their migratory capacity. Infect Immun. 2005, 73: 2564-2567.CrossRefPubMedPubMedCentral
21.
go back to reference Wu Q, Feng Y, Yang Y, Jingliu , Zhou W, He P, Zhou R, Li X, Zou J: Kinetics of the phenotype and function of murine peritoneal macrophages following acute inflammation. Cell Mol Immunol. 2004, 1: 57-62.PubMed Wu Q, Feng Y, Yang Y, Jingliu , Zhou W, He P, Zhou R, Li X, Zou J: Kinetics of the phenotype and function of murine peritoneal macrophages following acute inflammation. Cell Mol Immunol. 2004, 1: 57-62.PubMed
22.
go back to reference Turchyn LR, Baginski TJ, Renkiewicz RR, Lesch CA, Mobley JL: Phenotypic and functional analysis of murine resident and induced peritoneal macrophages. Comp Med. 2007, 57: 574-580.PubMed Turchyn LR, Baginski TJ, Renkiewicz RR, Lesch CA, Mobley JL: Phenotypic and functional analysis of murine resident and induced peritoneal macrophages. Comp Med. 2007, 57: 574-580.PubMed
23.
go back to reference Barral A, Pedral-Sampaio D, Grimaldi Júnior G, Momen H, McMahon-Pratt D, Ribeiro de Jesus A, Almeida R, Badaro R, Barral-Netto M, Carvalho EM: Leishmaniasis in Bahia, Brazil: evidence that Leishmania amazonensis produces a wide spectrum of clinical disease. Am J Trop Med Hyg. 1991, 44: 536-546.PubMed Barral A, Pedral-Sampaio D, Grimaldi Júnior G, Momen H, McMahon-Pratt D, Ribeiro de Jesus A, Almeida R, Badaro R, Barral-Netto M, Carvalho EM: Leishmaniasis in Bahia, Brazil: evidence that Leishmania amazonensis produces a wide spectrum of clinical disease. Am J Trop Med Hyg. 1991, 44: 536-546.PubMed
24.
go back to reference Saldanha Machado CJ, Tereza A, Filipecki P, Teixeira M: Current Brazilian law on animal experimentation. Science. 2009, 324: 1643-1644.CrossRefPubMed Saldanha Machado CJ, Tereza A, Filipecki P, Teixeira M: Current Brazilian law on animal experimentation. Science. 2009, 324: 1643-1644.CrossRefPubMed
25.
go back to reference Nibbering PH, Leijh PC, van Furth R: Quantitative immunocytochemical characterization of mononuclear phagocytes. II. Monocytes and tissue macrophages. Immunology. 1987, 62: 171-176.PubMedPubMedCentral Nibbering PH, Leijh PC, van Furth R: Quantitative immunocytochemical characterization of mononuclear phagocytes. II. Monocytes and tissue macrophages. Immunology. 1987, 62: 171-176.PubMedPubMedCentral
26.
go back to reference Lagasse E, Weissman IL: Flow cytometric identification of murine neutrophils and monocytes. J Immunol Methods. 1996, 197: 139-150.CrossRefPubMed Lagasse E, Weissman IL: Flow cytometric identification of murine neutrophils and monocytes. J Immunol Methods. 1996, 197: 139-150.CrossRefPubMed
27.
go back to reference Wu L, Li CL, Shortman K: Thymic dendritic cell precursors: relationship to the T lymphocyte lineage and phenotype of the dendritic cell progeny. J Exp Med. 1996, 184: 903-911.CrossRefPubMed Wu L, Li CL, Shortman K: Thymic dendritic cell precursors: relationship to the T lymphocyte lineage and phenotype of the dendritic cell progeny. J Exp Med. 1996, 184: 903-911.CrossRefPubMed
28.
go back to reference Pulendran B, Smith JL, Caspary G, Brasel K, Pettit D, Maraskovsky E, Maliszewski CR: Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proc Natl Acad Sci U S A. 1999, 96: 1036-1041.CrossRefPubMedPubMedCentral Pulendran B, Smith JL, Caspary G, Brasel K, Pettit D, Maraskovsky E, Maliszewski CR: Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proc Natl Acad Sci U S A. 1999, 96: 1036-1041.CrossRefPubMedPubMedCentral
29.
go back to reference Cook AD, Braine EL, Hamilton JA: The phenotype of inflammatory macrophages is stimulus dependent: implications for the nature of the inflammatory response. J Immunol. 2003, 171: 4816-4823.CrossRefPubMed Cook AD, Braine EL, Hamilton JA: The phenotype of inflammatory macrophages is stimulus dependent: implications for the nature of the inflammatory response. J Immunol. 2003, 171: 4816-4823.CrossRefPubMed
30.
go back to reference Ato M, Stäger S, Engwerda CR, Kaye PM: Defective CCR7 expression on dendritic cells contributes to the development of visceral leishmaniasis. Nat Immunol. 2002, 3: 1185-1191.CrossRefPubMed Ato M, Stäger S, Engwerda CR, Kaye PM: Defective CCR7 expression on dendritic cells contributes to the development of visceral leishmaniasis. Nat Immunol. 2002, 3: 1185-1191.CrossRefPubMed
33.
go back to reference Yen JH, Kong W, Ganea D: IFN- inhibits dendritic cell migration through STAT-1-mediated transcriptional suppression of CCR7 and matrix metalloproteinase 9. J Immunol. 2010, 184: 3478-3486.CrossRefPubMedPubMedCentral Yen JH, Kong W, Ganea D: IFN- inhibits dendritic cell migration through STAT-1-mediated transcriptional suppression of CCR7 and matrix metalloproteinase 9. J Immunol. 2010, 184: 3478-3486.CrossRefPubMedPubMedCentral
Metadata
Title
Leishmania amazonensis infection impairs dendritic cell migration from the inflammatory site to the draining lymph node
Authors
Micely DR Hermida
Priscila G Doria
Angela MP Taguchi
José O Mengel
Washington LC dos-Santos
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2014
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/1471-2334-14-450

Other articles of this Issue 1/2014

BMC Infectious Diseases 1/2014 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.